honeybees of asia - flemish2016.files.wordpress.com · studies on the biology of honeybees stem...
TRANSCRIPT
-
Honeybees of Asia
-
.
-
H.R. Hepburn l S.E. RadloffEditors
Honeybees of Asia
-
EditorsProfessor Dr. H.R. HepburnDepartment of Zoology and EntomologyRhodes UniversityGrahamstown 6140, South [email protected]
Professor Dr. S.E. RadloffDepartment of StatisticsRhodes UniversityGrahamstown 6140, South [email protected]
ISBN 978-3-642-16421-7 e-ISBN 978-3-642-16422-4DOI 10.1007/978-3-642-16422-4Springer Heidelberg Dordrecht London New York
# Springer-Verlag Berlin Heidelberg 2011This work is subject to copyright. All rights are reserved, whether the whole or part of the material isconcerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting,reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publicationor parts thereof is permitted only under the provisions of the German Copyright Law of September 9,1965, in its current version, and permission for use must always be obtained from Springer. Violationsare liable to prosecution under the German Copyright Law.The use of general descriptive names, registered names, trademarks, etc. in this publication doesnot imply, even in the absence of a specific statement, that such names are exempt from the relevantprotective laws and regulations and therefore free for general use.
Cover illustration: Pollen forager of Apis cerana on an ornamental flower (Portulaca oleracea) in thecentre of Hangzhou (Zhejiang, China). Photo: Nikolaus Koeniger
Cover design: WMXDesign GmbH, Heidelberg, Germany
Printed on acid-free paper
Springer is part of Springer ScienceþBusiness Media (www.springer.com)
-
In Memoriam
Eva Widdowson Crane
1912–2007
-
.
-
Preface
Studies on the biology of honeybees stem from ancient times, in both Asia and
Europe. However, published scientific works on the honeybees of both regions
gained unanticipated momentum on the heels of World War II and were boosted
exponentially by Sputnik a decade later. Since that time, 95% of all publications on
Asian and 99% on European honeybees were published. We believe that the
publication of the Ruttner’s monographs (1988, 1992) was further major stimuli
for research on Asian honeybees. Having just brought extraordinary clarity to the
“real” honeybees (Apis cerana, Apis dorsata, Apis florea, and Apis mellifera), soonafter Apis koschevnikovi, Apis andreniformis, Apis laboriosa, and Apis nigrocinctareappear in the literature. Some 50% of all literature on Asian honeybees follows
publication of Ruttner’s classic work. Another major impetus for increased research
on honeybees in Asia undoubtedly stems from the rather thorough cover given to
this literature by Eva Crane and colleagues through some 50 odd years of Apicul-
tural Abstracts.
Interestingly, the lion’s share of work on Asian honeybees is also historically
postcolonial in origin. It has also very largely resulted from the joint efforts of
Asian and Western scientists working in tandem. On the Asian side, this year, 2010,
also sees the 10th international conference of the Asian Apicultural Association, a
body that has both stimulated Asian colleagues and made Western ones warmly
received. Perusal of recent apicultural literature shows that East–West scientific
alliances are increasing rapidly and bearing substantial fruit.
This volume is presented as a monograph. Monographs are usually under-
stood to be complete and detailed expositions of a subject at an advanced
level. While we believe that we have achieved this end through the inclusion
of chapters by specialists in the field, it must be pointed out that while each
chapter shows a reasonable depth of understanding, nonetheless they clearly
indicate chasms in our knowledge of the honeybees of Asia. Much presented
here is completely new and has, as yet, not been published in journals. Com-
pared with the literature on western honeybees, that for Asia reveals very thin
coverage for honeybee physiology, biochemistry, genetics, and pathology. This
volume is a status quo report of what is known, and we fervently hope that this
vii
-
collation will provide stimuli to broaden the base of the biology of the Asian
honeybees.
Grahamstown, South Africa H.R. Hepburn
January 2011 S.E. Radloff
viii Preface
-
Contents
1 The Asian Species of Apis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1Sarah E. Radloff, H.R. Hepburn, and Michael S. Engel
2 Phylogeny of the Genus Apis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23Nikolaus Koeniger, Gudrun Koeniger, and Deborah Smith
3 Biogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51H.R. Hepburn and Sarah E. Radloff
4 Asian Honeybees and Mitochondrial DNA . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69Deborah R. Smith
5 Genetic Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95Catherine L. Sole and Christian W.W. Pirk
6 Biology of Nesting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109Mananya Phiancharoen, Orawan Duangphakdee, and H.R. Hepburn
7 Absconding, Migration and Swarming . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133H.R. Hepburn
8 Comparative Reproductive Biology of Honeybees . . . . . . . . . . . . . . . . . . . 159Gudrun Koeniger, Nikolaus Koeniger, and Mananya Phiancharoen
9 Pheromones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207Christian W.W. Pirk, Catherine L. Sole, and R.M. Crewe
10 Honeybees in Natural Ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215Richard T. Corlett
ix
-
11 The Pollination Role of Honeybees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227Uma Partap
12 Foraging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257D.P. Abrol
13 Energetic Aspects of Flight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293H.R. Hepburn, Christian W.W. Pirk, and Sarah E. Radloff
14 The Dance Language . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313Orawan Duangphakdee, H.R. Hepburn, and Jürgen Tautz
15 Diseases of Asian Honeybees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 333Ingemar Fries
16 Asian Honeybee Mites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347Natapot Warrit and Chariya Lekprayoon
17 Colony Defence and Natural Enemies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369Stefan Fuchs and Jürgen Tautz
18 Self-Assembly Processes in Honeybees: The Phenomenonof Shimmering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397Gerald Kastberger, Frank Weihmann, and Thomas Hoetzl
19 Interspecific Interactions Among Asian Honeybees . . . . . . . . . . . . . . . . . . 445Ming-Xian Yang, Ken Tan, Sarah E. Radloff, and H.R. Hepburn
20 Bibliography of the Asian Species of Honeybees . . . . . . . . . . . . . . . . . . . . . 473H.R. Hepburn and Colleen Hepburn
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 659
x Contents
-
Contributors
D.P. Abrol Division of Entomology, Sher-e-Kashmir University of AgriculturalSciences and Technology, Chatha, Jammu (J&K) 180 009, India, dharam_abrol@
rediffmail.com
Richard T. Corlett Department of Biological Sciences, National University ofSingapore, Singapore, Singapore 117543, [email protected]
R.M. Crewe Social Insect Research Group, Department of Zoology and Entomol-ogy, University of Pretoria, Pretoria 0002, South Africa, [email protected]
Orawan Duangphakdee Ratchaburi Campus, King Mongkut’s University ofTechnology, Thonburi, Bangkok 10140, Thailand, [email protected]
Michael S. Engel Division of Entomology, Natural History Museum, Universityof Kansas, 501 Crestline Drive-Suite #140, Lawrence, KS 66049-2811, USA,
Ingemar Fries Department of Ecology, Swedish University of AgriculturalSciences, Uppsala 750 07, Sweden, [email protected]
Stefan Fuchs Institut für Bienenkunde (Polytechnische Gesellschaft), FB Biowis-senschaften, Goethe-Universität Frankfurt am Main, Karl von Frisch Weg 2 61440,
Germany, [email protected]
H.R. Hepburn Department of Zoology and Entomology, Rhodes University,Grahamstown 6140, South Africa, [email protected]
Thomas Hoetzl Institute of Zoology, University of Graz, Graz, Austria, [email protected]
Gerald Kastberger Institute of Zoology, University of Graz, Graz, Austria,[email protected]
Nikolaus Koeniger Institut für Bienenkunde, (Polytechnische Gesellschaft) Fach-bereich Biowissenschaften Goethe Universität, Frankfurt a.M. Karl-von-Frisch-
Weg 2, 61440 Oberursel, Germany, [email protected]
xi
-
Gudrun Koeniger Institut für Bienenkunde (Polytechnische Gesellschaft), Fach-bereich Biowissenschaften, Goethe Universität, Frankfurt a.M, Karl-von-Frisch-
Weg 2, 61440, Oberursel, Germany, [email protected]
Chariya Lekprayoon Center of Excellence in Biodiversity, Department of Biology,Faculty of Sciences, Chulalongkorn University, Bangkok 10330, Thailand,
Uma Partap Honeybees Project, Sustainable Livelihoods and PovertyReduction Programme, International Centre for Integrated Mountain Development
(ICIMOD), PO Box 3226, Kathmandu, Nepal, [email protected]
Mananya Phiancharoen King Mongkut’s University of Technology Thonburi,Ratchaburi Campus, Bangkok 10140, Thailand, [email protected]
Christian W.W. Pirk Social Insect Research Group, Department of Zoologyand Entomology, University of Pretoria, Pretoria 0002, South Africa,
Sarah E. Radloff Department of Statistics, Rhodes University, Grahamstown 6140,South Africa, [email protected]
Deborah Smith Department of Ecology and Evolutionary Biology/Entomology,University of Kansas, Haworth Hall, 1200 Sunnyside Ave, Lawrence, KS 66045,
USA, [email protected]
Catherine L. Sole Social Insect Research Group, Department of Zoology andEntomology, University of Pretoria, Pretoria 0002, South Africa, clsole@zoology.
up.ac.za
Ken Tan Eastern Bee Research Institute of Yunnan, Agricultural University,Heilongtan, Kunming, Yunnan Province, People’s Republic of China, eastbee@
public.km.yn.cn
Jürgen Tautz BEE Group, Biozentrum, Universität Am Hubland, 97074Würzburg, Germany, [email protected]
Natapot Warrit Center of Excellence in Entomology, Department of Biology,Faculty of Sciences, Chulalongkorn University, Bangkok 10330, Thailand; Depart-
ment of Entomology, National Museum of Natural History, Smithsonian Institu-
tion, Washington, DC 20013, USA, [email protected]
Frank Weihmann Institute of Zoology, University of Graz, Graz, Austria, [email protected]
Ming-Xian Yang Department of Zoology and Entomology, Rhodes University,Grahamstown 6140, South Africa; Department of Zoology, Sichuan Agricultural
University, Yaan, People’s Republic of China, [email protected]
xii Contributors
-
.
-
Chapter 1
The Asian Species of Apis
Sarah E. Radloff, H.R. Hepburn, and Michael S. Engel
1.1 Introduction
The number of species of honeybees recognised over the last two and a half
centuries has varied quite considerably, following the original descriptions of
Apis mellifera (1758) by Linnaeus and Apis florea (1787), Apis cerana (1793)and Apis dorsata (1793) by Fabricius. In the nineteenth century, Frederick Smith(1854–1871) described some 20 additional species, often based on single speci-
mens; only his taxa Apis andreniformis (1858) and Apis nigrocincta (1861), how-ever, survived in honeybee systematics. Contemporaneously, Gerst€acker (1863)published the first comprehensive phylogenetic and taxonomic treatise on Apis, andreduced all previously described forms (except A. andreniformis and A. nigro-cincta, which he either missed or ignored) to only the original four Linnean andFabrician species. Although Smith (1865) subsequently presented his case for seven
species, the views of Gerst€acker (1863) prevailed into the twentieth century(Koschevnikov 1900–1905; Enderlein 1906; von Buttel-Reepen 1906).
Matters then rested for another half century, until Maa (1953) published an
abstruse monograph in which he introduced some 24 species of honeybees within
four genera. These taxa have subsequently been almost totally ignored in the apicul-
tural literature, and the historically older views of Gerst€acker (1863) have endureduntil relatively recently. During the years leading up to the publication of Ruttner’s
(1988) monograph, a search for East Asian honeybees (probably stimulated byMaa’s
S.E. Radloff
Department of Statistics, Rhodes University, Grahamstown 6140, South Africa
e-mail: [email protected]
H.R. Hepburn
Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa
e-mail: [email protected]
M.S. Engel
Division of Entomology, Natural History Museum, University of Kansas, 501 Crestline Drive-
Suite #140, Lawrence, KS 66049-2811, USA
e-mail: [email protected]
H.R. Hepburn and S.E. Radloff (eds.), Honeybees of Asia,DOI 10.1007/978-3-642-16422-4_1, # Springer-Verlag Berlin Heidelberg 2011
1
-
original paper) ensued, with Apis laboriosa re-announced (Sakagami et al. 1980),A. andreniformis re-established (Wu and Kuang 1986, 1987; Kuang 1983), Apiskoschevnikovi rediscovered (Mathew and Mathew 1988; Rinderer 1988) andA. nigrocincta re-entering the scene (Hadisoesilo and Otis 1996). Finally, Apisnuluensis was described as a new species (Tingek et al. 1996). When Ruttner(1992) subsequently published his natural history of honeybees, he included
A. laboriosa, A. andreniformis and A. koschevnikovi alongside the “traditional”four species. In the most recent taxonomy of honeybees, Engel (1999) applied a
phylogenetic species concept and accordingly regarded A. laboriosa and A. nuluensisas synonyms of A. dorsata and A. cerana, respectively – a view that has not beenwidely accepted by apiculturists, who have tended to employ alternate species
concepts (that is, either the biological species or the evolutionary species concepts).
Even now, the number of recognised species of honeybees remains in a state of flux.
Conceptualisation of species recognition also changed through the centuries,
from the Platonic concept, exemplified by Linnaeus, to the slow introduction of the
idea of a biological species, developed by Poulton (1908), Rensch (1929) and
Dobzhansky (1937) and subsequently widely promulgated by Huxley (1940) and
Mayr (1942). Indeed, today there are as many concepts for species recognition as
there are putative honeybee species, and the very system by which we recognise
biological units in nature is fiercely debated (e.g., Wheeler and Meier 2000).
Moreover, honeybee researchers have focussed almost exclusively on the oldest
of the currently used species concepts, the biological species concept.
Nonetheless, whether a species is diagnosed by population phenomena (the
biological species concept), evolutionary lineages (the evolutionary species con-
cept) or genealogical descent (the phylogenetic species concept), classification still
requires that species-specific characteristics be brought to bear in the circumscrip-
tion of species. Likewise, there have been several phylogenetic analyses conducted
(Deodikar 1960; Sakai et al. 1986; Sheppard and Berlocher 1989; Alexander 1991;
Garnery et al. 1991; Smith 1991; Petrov 1992; Willis et al. 1992; Engel and Schultz
1997; Engel 1999; Raffiudin and Crozier 2007; cf. Chap. 2), all based implicitly on
the correctness of the named species.
Following the non-Linnean views of DuPraw (1964), however, coupled with the
idea that sub-specific categories are untenable in a contiguous population (Wilson
and Brown 1951), Hepburn and Radloff attempted to bypass the problem of
classification by designating statistically defined populations of honeybees under
the new coinage of “morphoclusters” (Hepburn et al. 2001a, b, 2005; Radloff et al.
2005a, b, c, 2010). They have since accepted the arguments of Engel (personal
communication) that “morphoclusters” are really statistically defined “subspecies”
to which they had been inconsistently applying trinomial names. Here, we report
the results of a full multivariate morphometric analysis of the Asian species of Apisand correct the classification of Apis in accordance with the rules of the Interna-tional Code of Zoological Nomenclature.
The systematics of honeybees has also undergone a paradigm shift as earlier
evolutionary taxonomic methods and systems of organisation have become passé,
having been replaced by the contemporary emphasis on populations, the statistical
2 S.E. Radloff et al.
-
distribution of morphological characters and the reconstruction of evolutionary
lineages. Moreover, there has been no diagnostic account of the Asian species of
Apis since Maa (1953). Here, we present the analyses of the currently recognisedspecies of Apis: A. andreniformis, A. cerana, A. dorsata, A. florea, A. koschevni-kovi, A. laboriosa, A. mellifera, A. nigrocincta and A. nuluensis (noting thatlaboriosa and nuluensis are valid only under the antiquated biological speciesconcept). We combine metrical and descriptive morphological characters, DNA
characteristics (cf. Chap. 4), behaviour and nesting (cf. Chap. 6) so as to holisti-
cally define honeybee species and more easily identify them, either in an equipped
laboratory or under field conditions.
1.2 The Dwarf Honeybees
1.2.1 Identification of Apis andreniformis and Apis florea
The distinctness of both A. florea and A. andreniformis as unequivocal, validbiological species is now well established and rests on the cumulative knowledge
of the morphology of drone genitalia (Lavrekhin 1935; Ruttner 1975, 1988; Kuang
and Li 1985; Wu and Kuang 1986, 1987; Wongsiri et al. 1990; Chen 1993; Patinawin
and Wongsiri 1993), differences in nest structure (Thakar and Tonapi 1962; Dung
et al. 1996; Rinderer et al. 1996; cf. Chap. 6), chemical profiles of beeswax (Aichholz
and Lorbeer 1999, 2000; cf. Chap. 6), morphometrics (Jayavasti and Wongsiri 1992;
Rinderer et al. 1995), allozyme polymorphism (Nunamaker et al. 1984; Li et al. 1986;
Gan et al. 1991), mtDNA sequence divergences (Smith 1991; Willis et al. 1992;
Nanork et al. 2001; cf. Chap. 4), flight (Radloff et al. 2001; cf. Chap. 13), timing of
mating flights (Rinderer et al. 1993; Otis et al. 2001; cf. Chap. 8), sexual selection
(Baer 2005) and niche differences (Oldroyd et al. 1992; Booncham et al. 1995;
Rinderer et al. 2002; cf. Chap. 6). Several of these differences contribute to the
complete reproductive isolation between the two species (Koeniger and Koeniger
1991, 2000, 2001; Otis 1991; Dung et al. 1996; cf. Chap. 8).
Unfortunately, accurate identifications of the dwarf honeybees in the older
literature are often difficult to assess because the worker bees are morphologically
similar and the species are sympatric over a wide area that extends from north-
eastern India to Indochina (Otis 1996; cf. Chap. 3). Some of the historical
confusion between A. florea and A. andreniformis stems from the fact that theirclassification is based on workers, which do not show great morphological
differentiation. Moreover, the descriptions and taxonomic keys of Maa (1953)
were based on very limited numbers of specimens, and some of the purported
differences between the two species become blurred if many workers of a colony
are analysed.
The most reliable characteristics to rapidly distinguish A. florea and A. andre-niformis are as follows: in drones, the “thumb” of the bifurcated basitarsus of the
1 The Asian Species of Apis 3
-
hind leg, which in A. florea is much longer than that of A. andreniformis (Ruttner1988); the structure of the endophallus (Lavrekhin 1935; Wongsiri et al. 1990;
Koeniger 1991; cf. Chap. 8); the cubital index in worker bees, which, at about 3 in
A. florea, is significantly less than that in A. andreniformis, which is at about 6; thejugal-vannal ratio of the hindwing, which, at about 75 in A. florea is greater thanthat of A. andreniformis, at about 65; the abdominal tergite 2, which in A. andre-niformis is deeply punctate, unlike that in A. florea; and the marginal setae on thehind tibiae, which in A. florea are usually entirely white, while those in A. andre-niformis are dark-brown to blackish, in sclerotised, non-callow individuals.
Several subspecies, varieties, and nationes of A. florea, first described byFabricius (1787), have been described over the last two centuries (Engel 1999).
A. andreniformis was described by Smith (1858) as a species distinct fromA. florea (Fabricius 1787) but was usually included among the varieties orsubspecies of the latter for nearly a century, until its re-establishment as a species
by Maa (1953). Although A. andreniformis was often considered a subspecies ofA. florea, no sub-specific taxa have ever been proposed for A. andreniformis.Unfortunately, an unspecifiable number of specimens of A. andreniformis mayhave been misidentified as A. florea during this period. All named forms wereeventually resolved into colour variants from widely separated localities (Dover
1929). Subsequently, Maa (1953) synonymised all previous such taxa of earlier
workers (Gerst€acker 1863; Enderlein 1906; von Buttel-Reepen 1906; Cockerell1911; Dover 1929), and no sub-specific categories of A. florea have been proposedsince then (Hepburn et al. 2005).
The mistaken notion that abdominal tergites 1 and 2 of A. florea are reddish andother segments at least partially reddish, while those of A. andreniformis areuniformly black, still permeates the literature. However, an inspection of several
hundred workers from several different colonies of each species quickly demon-
strates the extreme variation in pigmentation. This precludes these characters as a
useful distinguishing trait – a point actually recognised rather long ago (Drory
1888; Dover 1929). Finally, the combs of the two species are very different
(Rinderer et al. 1996; cf. Chap. 6). Full bibliographies of the literature on A. floreaand A. andreniformis are given in Hepburn and Hepburn (2005, 2009), respectively;cf. Chap. 20).
1.2.2 Apis andreniformis F. Smith (1858)
A. andreniformis, the smallest of the honeybees, has been studied far less thanA. florea. To date, there has been a single univariate morphometric comparisonof A. andreniformis from southeastern Thailand and Palawan Island in the Philippines(Rinderer et al. 1995). These two widely separated populations (~3,000 km)
differed only in a few characters that related to wing and metatarsal lengths,
which indicates that it is likely a very homogeneous species. Likewise, estimates
of the mtDNA haplotype divergence within the species was about 2% for A. florea
4 S.E. Radloff et al.
-
and 0.5% for A. andreniformis, indicating rather homogeneous populations in bothcases (Smith 1991; cf. Chap. 4).
The only published multivariate morphometric analysis of this species is the
recent study of Rattanawannee et al. (2008), who collected 67 colonies throughout
Thailand – 30 of which were for morphometric analysis and the remaining 37 for
DNA polymorphism. Twenty characters were used to assess morphometric varia-
tion. Principal component analysis yielded four factor scores, which, when plotted,
formed a single group, supported by a dendrogram generated from the cluster
analysis. Using linear regression analysis, Rattanawannee et al. (2008) demon-
strated the clinal pattern of morphometric characters, wherein body size decreases
from west to east, associated with decreasing altitude, while it increases from south
to north, associated with increasing altitude. Genetic variation, however, based on
the sequence analysis of the cytochrome oxidase subunit b, yielded two groups – a
result taken as tentative, pending more extensive analyses across the whole area of
distribution of A. andreniformis (cf. Chap. 3).
1.2.3 Apis florea Fabricius (1787)
Several univariate morphometric studies on regional or country bases have
appeared through the years, but they have not affected the taxonomy of the species.
In the first multivariate morphometric analysis of A. florea, Ruttner (1988) had onlylimited material, from geographically non-contiguous regions. Although the data
were insufficient for a comprehensive analysis, Ruttner (1988) demonstrated geo-
graphic variability and obtained three morphoclusters for A. florea. Recently,Tahmasebi et al. (2002) analysed A. florea and defined two morphoclusters froma geographical continuum in Iran. Combining their data with that of Ruttner (1988)
and Mogga and Ruttner (1988), they also reported three morphoclusters for all
A. florea; but again, a lack of geographical contiguity applies to these data as well.A multivariate study of the A. florea of Thailand has also been conducted (Chaiya-wong et al. 2004). The raw data of Ruttner (1988), Tahmasebi et al. (2002), Mogga
and Ruttner (1988) and Chaiyawong et al. (2004) were included in a subsequent
study in which previous gaps in the distribution had been filled, finally allowing a
comprehensive morphometric database for A. florea over its entire distribution to becompiled (Hepburn et al. 2005).
Principal component, discriminant and cluster analyses using the single linkage
(nearest neighbour) procedure were carried out and produced a dendrogram of three
main clusters (Fig. 1.1). Phenetically, cluster 1 initially linked colonies from
Myanmar and Thailand, followed by Cambodia and finally Northern Vietnam;
cluster 2 initially linked colonies from Oman, North India and Nepal, followed by
those from South India; cluster 3 linked colonies from Iran and Pakistan; while
clusters 2 and 3 linked colonies from Southern Vietnam (Fig. 1.1).
Radloff and Hepburn (1998, 2000) and Hepburn et al. (2001b) established
empirically that the greater the sampling distances between localities, the greater
1 The Asian Species of Apis 5
-
the likelihood that artefactual morphoclusters would emerge in multivariate ana-
lyses. Conversely, where between-group variation is larger than within-group
variation, biometric subgroups falling within smaller geographic domains may be
swamped and obscured. Radloff et al. (2003b) also established the statistical
significance of both colony sample size and individual bee sample size to studies
of honeybee populations. These principles are particularly useful in the analyses of
previous studies of A. florea and explain why Tahmasebi et al. (2002) defined twomorphoclusters when they analysed the A. florea of Iran. Combining their data withthat of Ruttner (1988) and Mogga and Ruttner (1988), Radloff et al. (2003b)
reported three morphoclusters. In both studies, however, there was still a lack of
geographical contiguity in the samples and each of the three groups was separated
by intervals of about 3,000 km. When Hepburn et al. (2005) analysed the bees from
the whole spectrum of localities sampled, the clinal nature of the morphometric
measurements of the species became readily apparent. Precisely this same pattern
was obtained in studies of A. cerana (Radloff et al. 2010).On a mesoscale level, there have been several regional studies of morpho-
metric variation in A. florea in India and Iran, representing sampling intervals ofabout 3,000 km. In northwestern India and eastern Pakistan, extending along a
north–south transect between 25� and 32�N latitude, a transition in the popula-tions occurs. There are significant interlocality differences in both the mean
values of morphometric characters and their coefficients of variation, for most
Iran
Pakistan
Single LinkageEuclidean distances
Linkage Distance
Oman
N. India
S. India
S. Vietnam
N. Vietnam
Myanmar
Thailand
Cambodia
Nepal
0.2 0.4 0.6 0.8 1.0 1.2
Fig. 1.1 Hierarchical clustering dendrogram for Apis florea, derived from single linkage cluster-ing on morphometric characters: length of femur (5); length of tibia (6); length of metatarsus (7);
tergite 3; longitudinal (9); tergite 4; longitudinal (10); length of forewing (17); wing angle G18
(25), averaged for countries. The original coded numbers assigned to these characters by Ruttner
(1988)
6 S.E. Radloff et al.
-
characters measured (Narayanan et al. 1960; Bhandari 1983; Sharma 1983) –
implying heterogeneity in the population. Likewise, at hotter, drier and lower
latitudes, A. florea are smaller than those at cooler and higher latitudes, leadingto the proposition of possibly different ecotypes associated with climate at
particular latitudes (Narayanan et al. 1960; Bhandari 1983). There are, however,
alternative views on this point (Sharma 1983). Within a sample from India,
Hepburn et al. (2005) obtained a strong, significant positive correlation between
altitude and the principal component variables that reflect size. This pattern
might benefit from additional attention.
Tahmasebi et al. (2002) reported an analysis of A. florea from 26 localities in Iranand obtained two morphoclusters: a western group of larger bees at higher latitudes
(29–34�) and a lower latitude group of smaller bees to the east (
-
1.3.2 Apis cerana Fabricius (1793)
Over the last two decades, great strides have been made following Ruttner’s (1988)
first multivariate analysis of this species. Subsequent authors used Ruttner’s inter-
pretations of A. cerana as a new baseline and concentrated on morphoclustersderived from multivariate analyses on a microscale level (Muzaffar and Ahmad
1989; Pesenko et al. 1989; Rinderer et al. 1989; Otis and Hadisoesilo 1990; Singh
et al. 1990; Sulistianto 1990; Szabo 1990; Ono 1992; Verma 1992; Verma et al.
1994; Hadisoesilo and Otis 1996; Fuchs et al. 1996; Damus and Otis 1997;
Sylvester et al. 1998) as well as on a more regional, mesoscale level (Yang 1986,
2001; Peng et al. 1989; Diniz-Filho et al. 1993; Damus and Otis 1997; Tilde et al.
2000; Hepburn et al. 2001a, b; Kuang 2002; Radloff and Hepburn 2002; Smith
2002; Tan et al. 2003; Radloff et al. 2003a, 2005a, b, c).
Historically, unravelling the structural complexity of A. cerana (Fabricius 1793)has been a continuous process, the details of which were recently given by Radloff
et al. (2010). They reported the first multivariate morphometric analysis of A.cerana across its full geographical range and identify the statistically definablemorphoclusters and subcluster populations within them. Principal component (PC)
plots, using both the first and second PC scores and the first and third PC scores, did
not reveal distinct morphoclusters. However, a substructuring of the PC plots was
obtained by introducing local labelling and running a hierarchical cluster analysis,
using the mean scores for PC 1 to 3 to identify homogeneous morphoclusters. This
approach revealed six main morphoclusters, which were defined (Radloff et al.
2010) as follows (cf. Fig. 3.3):
1. Morphocluster I, “Northern cerana”, which extends from northern Afghanistanand Pakistan through northwest India, across southern Tibet, northern Myanmar,
China and northeasterly into Korea, far eastern Russia and Japan. Six subclusters
or populations are morphometrically discernible within this morphocluster (a) an
“Indus” group in Afghanistan, Pakistan and Kashmir; (b) a “Himachali” group
in Himachal Pradesh, India; (c) an “Aba” group in Ganshu and Sichuan provinces
in China, northern China and Russia; (d) a subcluster in central and eastern
China; (e) a “southern cerana” subcluster in southern Yunnan, Guangdong,Guangxi and Hainan in China and (f) a “japonica” group in Japan and Korea.
2. Morphocluster II, “Himalayan cerana”, which includes the bees of northernIndia and some of southern Tibet and Nepal. Two subclusters are discernible
within this morphocluster: the bees of the northwest, which are termed the
“Hills” group, and those of the northeast, termed the “Ganges” group (cf.
Figs. 3.1 and 3.3).
3. Morphocluster III, “Indian plains cerana”, which occurs across the plains ofcentral and southern India and Sri Lanka as a fairly uniform population, long
known as “plains cerana” in this subcontinent (cf. Figs. 3.1 and 3.3).4. Morphocluster IV, “Indo-Chinese cerana”, which forms a compact group in
Myanmar, northern Thailand, Laos, Cambodia and southern Vietnam (cf.
Figs. 3.1 and 3.3).
8 S.E. Radloff et al.
-
5. Morphocluster V, “Philippine cerana”, which is restricted to the Philippines, butwith the exclusion of most of Palawan Island, which instead groups with mor-
phocluster VI. Within these islands, there are subclusters, and these bees are
termed after the major island groups located there: “Luzon” bees, “Mindanao”
bees and “Visayas” bees. The latter two subclusters show closer morphometric
similarity than the former (cf. Figs. 3.1 and 3.3).
6. Morphocluster VI, “Indo-Malayan cerana”, which extends from southern Thailand,through Malaysia and Indonesia. This large area consists of a rather morpho-
metrically uniform bee, below the South China Sea. Three subclusters are dis-
cernible within this morphocluster: (a) Palawan (Philippines) and Borneo bees;
(b) Malay Peninsula, Sumatera and some Sulawesi bees; and (c) Indonesia (Java,
Bali, Irian Jaya, some Sulawesi and Sumatera) bees (cf. Figs. 3.1 and 3.3).
We must now consider how these results relate to earlier geographically large-
scale analyses. When all of the mesoscale morphoclusters of Radloff et al. (2010)
are compared with the new macroscale results, the only discrepancies are that, in
the former, (1) the bees of the Philippines were included with those of Indonesia
and Borneo; and (2) the bees of Japan are now placed in the Northern Asia
morphocluster of the latter. However, there are differences between the mapped
morphocluster results of Ruttner (1988) and Damus and Otis (1997) and those of
Radloff et al. (2010). These discrepancies are best explained by the sampling
differences in each study, which affected the degree of morphometric discrimina-
tion of the honeybees of Japan.
Ruttner (1988) had access to only a very small sample of large A. cerana fromChina and none from Russia. The only morphocluster I bees available to him were
from the far northwest of the A. cerana range (Afghanistan and Pakistan) and some6,000 km distant from Japan – the bees of which form a subcluster in a continuum
of A. cerana morphocluster I. Gaps in the sampling inevitably resulted in thedifferences between Afghani and Japanese A. cerana being artefactually magnified.The dataset of Damus and Otis (1997) was based on the much smaller bees of the
more southerly oceanic islands (Philippines, Indonesia, Borneo, etc.) with the same
effect.
Returning to the matter of sampling, many thorough multivariate studies of
A. cerana, sampled at a microscale basis, had been published; but, with theadvantage of hindsight, the effects of limited sampling are evident. An important
series of papers was published on sub-Himalayan A. cerana; however, the areassampled were widely separated, and the net result was discrimination of seven
distinct morphoclusters (Singh et al. 1990; Verma 1992; Verma et al. 1994). When
the original data from all these papers were subsequently combined into a much
larger dataset in collaboration with those authors, and for which the previous geo-
graphical gaps were filled, the newer multivariate analysis (now on a geographical
continuum in the sub-Himalayan region) yielded only four morphoclusters for the
same region – two of which contained biometric subclusters (Hepburn et al. 2001b).
Analysis of the A. cerana of the western sub-Himalayas yielded an additionalHindhu Kush morphocluster, bringing the Himalayan string of morphoclusters to
1 The Asian Species of Apis 9
-
five (Radloff et al. 2005a). The analysis found that high variance domains occur at
the edges of the morphoclusters and biometric subclusters. The bees decrease in
size from west to east, but increase in size with increasing altitude. When analyses
were subsequently extended from Afghanistan to Vietnam, covering all of south-
ern-mainland Asia, scores from the principal components analysis yielded five
statistically identifiable morphoclusters (Radloff et al. 2005b). At this continental
resolution, the five morphoclusters previously obtained in the regional analyses
of the Himalayan string (Hepburn et al. 2001b; Radloff et al. 2005a) were reduced
to three, which were also coherently distributed with the different climatic zones of
the region (Radloff et al. 2005b).
In a parallel series of studies on the A. cerana of China, Tan et al. (2002, 2003)showed that bees from the northern high-altitude areas of Yunnan Province were
clearly larger and darker and showed similarities to samples from Beijing, Nepal
and northern India, whereas bees from southern Yunnan clustered with the bees of
Thailand and Vietnam. These results were completely consistent with those of
Radloff et al. (2005b) for the bees of southern Yunnan. Morphometric analyses of
A. cerana from oceanic Asia yielded two distinct morphoclusters, bringing the thentotal number of morphoclusters to seven (Radloff et al. 2005c). On completion of
the above series of regional mesoscale studies, the newly formed comprehensive
dataset for all A. cerana was subjected to multivariate morphometric analysis. Thefinal result was that six distinct morphoclusters of A. cerana were obtained, asdiscussed above (Radloff et al. 2010; cf. Fig. 3.3).
1.3.3 Apis koschevnikovi Enderlein (1906)
A. koschevnikovi was originally described by Enderlein (1906) as “Apis indicavariety koschevnikovi” and by von Buttel-Reepen (1906) as “Apis mellifica indicavariety koschevnikovi”. Authorship for this species has however been formallyassigned to Enderlein (Engel 1999) as A. koschevnikovi Enderlein (1906), inaccordance with nomenclatural practice. With few exceptions (Maa 1953; Goetze
1964), there were no accounts of A. koschevnikovi until its rediscovery eightdecades later in Borneo (Mathew and Mathew 1988; Rinderer 1988; Tingek et al.
1988). However, A. koschevnikovi had indeed been widely collected in the Sunda-land region of Southeast Asia during the interim, as evidenced by collections in
various museums (Otis 1996). In a recent flurry of publications (Hepburn and
Hepburn 2008), it has been established that A. koschevnikovi is a morphometricallydistinct species (Tingek et al. 1988; Rinderer et al. 1989; Ruttner et al. 1989;
Sulistianto 1990; Hadisoesilo et al. 1999), reproductively isolated (Koeniger et al.
1996c) and differing in both nuclear and mitochondrial DNA regions (Arias et al.
1996; Takahashi et al. 2002; Raffiudin and Crozier 2007) from other species of
Apis, with which it has a sympatric distribution.Although most characters of length are some 10–15% greater in worker honey-
bees of A. koschevnikovi than in A. cerana (Rinderer et al. 1989; Sulistianto 1990),
10 S.E. Radloff et al.
-
these species may be confused in alcohol-preserved specimens that do not show the
natural reddish-yellow brightness of the former. Multivariate analyses of A.koschevnikovi samples from Malaysia, Borneo and Indonesia clearly establishedthat this species is comprised of a single morphocluster (Hadisoesilo et al. 2008).
Moreover, the morphocluster can be delimited with as few as 12 morphological
characters. It would also appear to be a very homogeneous species, in comparison
with A. cerana, over the same area of distribution, because the average coefficientof variation in A. koschevnikovi is 1.8%, while in A. cerana, it is 4.3% for the samecharacters (Hadisoesilo et al. 2008).
1.3.4 Apis nigrocincta F. Smith (1861)
The life history of A. nigrocincta F. Smith (1861) is curiously similar to that ofA. koschevnikovi. Described as a new species by F. Smith (1861), it remainedvirtually unreported, with a few exceptions, for more than a century, until it was
re-examined in the 1990s. In the first instance, Hadisoesilo et al. (1995) detected
two distinct groups of honeybees in Sulawesi, Indonesia. A discriminant analysis of
these bees showed one group to be A. cerana and the other as neither A. cerana norA. koschevnikovi. Moreover, these then unidentified bees appeared similar toA. nigrocincta when compared to the holotype. In rapid succession, the Guelphgroup confirmed that the unknown bees were indeed A. nigrocincta and that theyoccur in the Philippines as well (Damus and Otis 1997). Further multivariate
analyses confirmed that A. nigrocincta occurred in western Sulawesi, MindanaoIsland in the Philippine chain and on Sangihe Island, situated between the two
(Damus and Otis 1997).
Studies of drone flight times further supported the status of A. nigrocincta as aspecies distinct from A. cerana (Hadisoesilo and Otis 1996; Otis et al. 2001).Interestingly, they found no differences in the drone genitalia of A. nigrocinctaand A. cerana. The reality of A. nigrocincta as a valid species continued to growwhen it was shown that the cappings of drone cells in A. nigrocincta lacked thewell-known pore that is present in A. cerana (Hadisoesilo and Otis 1998). Jayavastiand Wongsiri (1992) were able to differentiate A. nigrocincta and A. cerana on thebasis of sting morphology, while Keeling et al. (2001) established species-specific
differences in the mandibular gland pheromones of queens. The species was also
recognised in taxonomic studies of Apis by Engel (1999).Shortly afterwards, the separation of these species through mtDNA analyses
(Smith et al. 2000), receptor gene sequences (Raffiudin and Crozier 2007) as well as
new haplotypes for the non-coding region of mtDNA (Takahashi et al. 2002)
confirmed the A. nigrocincta species. More recent analyses of nuclear and mito-chondrial DNA sequences further support the validity of A. nigrocincta (Arias andSheppard 2005). Finally, Raffiudin and Crozier (2007) supported A. nigrocincta asa valid species on the basis of general biology, DNA, acoustics, waggle dance and
combs.
1 The Asian Species of Apis 11
-
Only in the last decade have we acquired sufficient evidence to consider A.nigrocincta as a reasonably well-defined valid species. Hadisoesilo and Otis (1996)and Otis et al. (2001) demonstrated that, although sympatric with A. cerana, A.nigrocincta is reproductively isolated from other Asian Apis species in the timing ofits mating flights, is distinguishable from other Apis species in morphometricanalyses (Hadisoesilo et al. 1995; Hadisoesilo and Otis 1996) and differs in
mtDNA haplotypes (Smith et al. 2000, 2003). However, until very recently, its
known distribution was limited to Indonesia and the Philippines (Otis 1996).
Interestingly, Otis (1996) suggested that A. nigrocincta might have been derivedfrom China, because it shares closer similarities with A. cerana from the mainlandthan from the southwest.
1.3.5 Apis nuluensis Tingek et al. (1996)
Just over a decade ago, Tingek et al. (1996) collected bees at flowers on Gunung
Emas at an altitude of about 2,000 m, which appeared distinctly different from
A. cerana and A. koschevnikovi. They conducted morphometric measurements onthese blackish bees, using most of Ruttner’s (1988) characters, and showed that
they differed significantly from A. cerana and A. koschevnikovi workers and drones(with which they are sympatric), and accordingly described these bees as a new
species, A. nuluensis. More extensive measurements were reported by Fuchs et al.(1996), who found that, in a principal component analysis plotting the first three of
the axes derived from principal components, A. nuluensis was clearly separatedfrom the other sympatric Asian Apis species. Moreover, a hierarchic cluster analy-sis of group centroids in canonical function space clearly showed that A. nuluensisis quite distinctly separated from the other species.
While the above remarks are restricted to inferences based entirely on morpho-
metrics, other biological observations were soon brought to bear on the legitimacy
of A. nuluensis as a distinct species under the biological species concept. Koenigeret al. (1996a, b) observed that the drone mating flight period was temporally
completely isolated from those of A. cerana and A. koschevnikovi. Although thereis a very small window of temporal overlap between A. nuluensis and A. cerana, thephysical differences between the two would be adequate to obviate any hetero-
specific mating. This separation in time is a pre-mating barrier that provides
complete reproductive isolation among the honeybees with which it is sympatric
(Koeniger et al. 1996a, b; cf. Chap. 8).
Although A. nuluensis was initially proposed on the basis of morphological andbehavioural characters, Arias et al. (1996) analysed variable sites for the ND2
mitochondrial gene as well as for the intron of EF-1a – the results of which indicatethat A. nuluensis and A. cerana are closely related or even that the former wasderived from the latter, which challenges the validity of the species under more
modern species concepts, such as the phylogenetic species concept. They con-
cluded that A. nuluensis diverged from A. cerana more recently than did
12 S.E. Radloff et al.
-
A. koschevnikovi. Using a slightly different approach, Takahashi et al. (2002) andTanaka et al. (2001) investigated the haplotypes for the non-coding region of
mitochondrial DNA and reached essentially the same conclusion as Arias et al.
(1996). Similarly, on the basis of morphometrics, Fuchs et al. (1996) concluded
that A. nuluensis shares a greater similarity with A. cerana than with A. koschevni-kovi. A. nuluensis is thus far known only from montane forests on the Gunung Emasin Sabah State, Malaysian Borneo. This area is at the northeastern tip of mountain
ranges that extend continuously for about 1,000 km to the southwest, along a spine of
mountains that extends two-thirds the length of Borneo. The region is remote,
sparsely inhabited and not readily accessible. It seems highly likely that A. nuluensisoccurs along this spine.
1.4 The Giant Honeybees
1.4.1 Apis dorsata Fabricius (1793)
The classification of the giant honeybees, A. dorsata and A. laboriosa, has longbeen problematical. The former was described by Fabricius in 1793 and various
forms were introduced between then and the time of Maa (1953). Maa recorded the
various synonymies that had previously arisen and then reshaped and split the
species into A. breviligula (one specimen from the Philippines), A. binghami(Sulawesi, formerly the Celebes) and A. dorsata (the wider distribution as knowntoday). Over the next three decades, however, none of the names proposed by Maa
(1953) appeared in the apicultural literature in any form other than “A. dorsata”.The next important discussion of these bees was that of Ruttner (1988), who
noted that the standard deviations of several morphometric characters, representing
widely separated localities were very small indeed so that A. dorsata appeared veryhomogeneous. He further argued that differences regarded by some as species-
specific in the A. dorsata group are of the same order of magnitude as those usedto discriminate subspecies of A. mellifera. Acknowledging some unusual aspects ofthe biology of A. laboriosa, Ruttner (1988) nonetheless was not prepared torecognise this bee as a clear-cut species, especially in the light of the report that
no differences could be found in the male genitalia of A. dorsata and whatpurported to be “A. laboriosa” (McEvoy and Underwood 1988). He did, however,support the subspecies of A. d. binghami, A. d. breviligula and A. d. dorsata. A. d.breviligula is a conspicuously short-tongued bee of the Philippines, whose beha-viour differs in important respects from A. d. dorsata. Congregations of severalnests, common in areas of the latter, do not occur in those of the former; likewise,
seasonal migration, also common in the former, is absent from the latter (Morse and
Laigo 1968). A. d. binghami is a long-tongued, long-winged form, also isolated atthe periphery of A. dorsata distribution in Sulawesi. Whether peripheral isolatesshould be considered as taxonomically distinct is a matter that is open to debate
(Lo et al. 2010).
1 The Asian Species of Apis 13
-
The history of works on A. dorsata once again illuminates the problem of samplesize. When the spectrum of sampling has been wide, even though it contains many
geographical gaps, it may be that a species seems rather homogeneous; and so it
appeared to Ruttner. Prior to Ruttner (1988), however, many smallish and prelimi-
nary investigations had been reported. Most such studies emanated from India
(Ratnam 1939; Deodikar 1959a, b, Deodikar et al. 1977; Trehan and Singh 1961;Jain 1967; Kshirsagar 1969; Sharma 1983; Bhandari 1983; Mujumdar and Kshir-
sagar 1986; Singh et al. 1990) and revolved around populations of northwest India,
where great variations in altitude occur. All of these studies on the morphometrics
and population structure of A. dorsata demonstrated that the populations sampledshowed significant interlocality variation, which attests to the heterogeneity of
these bees. Similar results were reported elsewhere (Kuang 1986). Unfortunately,
there has not been any comprehensive multivariate morphometric analysis over the
entire range of A. dorsata to date. However, it may well eventuate that theinferences from nuclear and mitochondrial DNA sequence data will prove more
informative than those derived from morphometrics (Arias and Sheppard 2005; cf.
Chap. 4).
In any event, over the last century, there have been only three “pre-biological
species” taxonomic systematists (Enderlein 1906; von Buttel-Reepen 1906; Maa
1953) and two post-Huxley systematists (Daly 1985; Engel 1999) within honeybee
systematics. Engel (1999) is the only contemporary systematist working on honey-
bees who presents both usage views: one in which there exists only A. dorsata andthe other in which there exist A. d. binghami, A. d. breviligula and A. d. dorsata. Thepractice among honeybee biologists has, however, been to use the trinomial epithet
as a tool on which to simply apply their names, based on inferences about the
magnitude of differences they encounter. In these circumstances, the post-Ruttner
apicultural literature abounds with the names A. d. binghami, A. d. breviligula andA. d. dorsata, as well as A. laboriosa. More recently, the names A. binghami,A. breviligula and A. dorsata, as well as A. laboriosa, are beginning to appear incommon usage within the literature, which may reflect a growing consensus on the
matter under certain species concepts (Lo et al. 2010). It would appear that total
evidence and quantitative approaches, uniting multiple, independent lines of evi-
dence, will be needed in place of morphometrics in the circumscription of species
for this particular group of bees.
1.4.2 Apis laboriosa F. Smith (1871)
Like other lesser-known species of honeybees, the Himalayan A. laboriosaremained virtually unreported for a century after its original description by
F. Smith (1871). While von Buttel-Reepen (1906) listed it as a subspecies of
A. dorsata, Maa (1953) effectively resurrected its species status. More recently,Engel (1999) referred to A. laboriosa somewhat equivocally as A. dorsata laboriosabut did not accord it species status when applying a phylogenetic species concept.
14 S.E. Radloff et al.
-
Under both the biological and evolutionary species concepts, this form is considered
a valid species and a recognised taxonomical entity. Real interest in A. laboriosagained momentum following a major morphometric and biogeographical analysis by
Sakagami et al. (1980). They established unequivocally that it was different from
A. dorsata in 96 of 103 different morphometric measurements but, surprisingly,remained somewhat equivocal as to its taxonomical status. Li (1984), Chen (1993)
and Trung et al. (1996) also distinguished the two species morphologically. McEvoy
and Underwood (1988) argued, somewhat tenuously, that A. laboriosa and A. dorsataare sound species, based on the fact that no morphologically intermediate forms were
known. These two species are very rarely sympatric, withA. dorsata usually occurringbelow altitudes of 1,500 m and A. laboriosa between altitudes of 2,500 and 4,000 m(Roubik et al. 1985; Allen 1995; Otis 1996; Thapa et al. 2001).
Nonetheless, a general consensus that A. laboriosa is a well-defined species underthe biological species concept, developed only after (1) Li et al. (1986) and Kuang
and Li (1988) clearly separated A. laboriosa from A. dorsata and other Apis speciesby their esterase isozyme profiles; (2) Underwood (1990) showed that A. laboriosaand A. dorsata are reproductively separated by drone mating flight times; (3) Blumet al. (2000) reported that no common chemical constituents were found in analyses
of the cephalic and abdominal secretions of A. laboriosa and A. dorsata; (4) Aichholzand Lorbeer (1999, 2000) showed that the chemical profile of A. laboriosa beeswaxdiffers unequivocally from that of all other Apis; (5) Kirchner et al. (1996) showedthat, unlike A. dorsata, there is no acoustic component of the waggle dance inA. laboriosa and (6) Woyke et al. (2008) identified their differences in defensivebehaviour. Sequence divergence between A. laboriosa and A. dorsata was consistentwith behavioural data and supports the species status of A. laboriosa under thebiological species concept (cf. Chap. 4).
1.5 Conclusion
Phylogenetic analyses strongly supported the basic topology that is recoverable
from morphometric analysis, which groups the honeybees into three major clusters:
giant bees (A. dorsata, A. binghami and A. laboriosa), dwarf bees (A. andreniformisand A. florea) and cavity-nesting bees (A. mellifera, A. cerana, A. koschevnikovi,A. nuluensis and A. nigrocincta). The clade of Asian cavity-nesting bees, however,included paraphyletic taxa. Exemplars of A. cerana collected from divergent por-tions of its range were less related to each other than were the sympatric taxa,
A. cerana, A. nuluensis and A. nigrocincta. Nucleotide sequence divergencebetween allopatrically distributed western (A. mellifera) and eastern (A. cerana,A. koschevnikovi, A. nigrocincta and A. nuluensis) cavity-nesting species (beingaround 18% for the mitochondrial gene and 10–15% for the nuclear intron)
suggested an earlier divergence for these groups than previously estimated from
both morphometric and behavioural studies.
1 The Asian Species of Apis 15
-
This latter finding necessitates a re-evaluation of the hypothesised origin of
extant European, African and West Asian A. mellifera. In addition, the growingevidence of honeybee diversity in the geological past is not only expanding the total
number of species but also forcing a reconsideration of global Apis biogeography.By example, the recent discovery of fossil honeybees in North America expands the
lineage natively into the New World (Engel et al. 2009). The discovery of giant
honeybees in Japan during the Miocene, demonstrates how, under changing cli-
mates, lineages considerably expanded their historical ranges (Engel 2006). Per-
haps most interestingly, the diversity of basal fossil species currently suggests a
more western origin for the honeybees, with a subsequent invasion and rapid
radiation across Asia, which resulted in the remarkable array of species and
challenging forms we see today.
References
Aichholz R, Lorbeer E (1999) Investigation of combwax of honeybees with high-temperature gas
chromatography and high-temperature gas chromatography-chemical ionization mass spec-
trometry. I. High-temperature gas chromatography. J Chromatogr A 855:601–615
Aichholz R, Lorbeer E (2000) Investigation of combwax of honeybees with high-temperature gas
chromatography and high-temperature gas chromatography-chemical ionization mass spec-
trometry. II. High-temperature gas chromatography-chemical ionization mass spectrometry.
J Chromatogr A 883:75–88
Alexander BA (1991) Phylogenetic analysis of the genus Apis (Hymenoptera: Apidae). AnnEntomol Soc Am 84:137–149
Allen MF (1995) Bees and beekeeping in Nepal. Bee World 76:185–194
Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae;
Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol
37:25–35
Arias MC, Tingek S, Kelitu A, Sheppard WS (1996) Apis nuluensis Tingek, Koeniger andKoeniger, 1996 and its genetic relationship with sympatric species inferred from DNA
sequences. Apidologie 27:415–422
Baer B (2005) Sexual selection in Apis bees. Apidologie 36:187–200Bhandari VC (1983) Biometrical studies on Apis florea F and Apis dorsata F of northwestern India.
Thesis, Himachal Pradesh University, Simla
Blum MS, Fales HM, Morse RA, Underwood BA (2000) Chemical characters of two related
species of giant honeybees (Apis dorsata and A. laboriosa): possible ecological significance.J Chem Ecol 26:801–807
Booncham U, Wongsiri S, Thirakupt K (1995) Niche differences between A. florea andA. andreniformis in dry-evergreen forest, Thailand. In: International Conference on TropicalBees Environment, Pedu Lake, Kedah, p 33
Chaiyawong T, Deowanish S, Wongsiri S, Sylvester HA, Rinderer TE, de Guzman L (2004)
Multivariate morphometric study of Apis florea in Thailand. J Apic Res 43:123–127Chen YC (1993) Apiculture in China. Agricultural Scitech Publishing House of China, Beijing
Cockerell TDA (1911) Descriptions and records of bees XXXV. Ann Mag Nat Hist 8:310–319
Daly HV (1985) Insect morphometrics. Annu Rev Entomol 30:415–438
Damus MS, Otis GW (1997) A morphometric analysis of Apis cerana F. and Apis nigrocinctaSmith populations from Southeast Asia. Apidologie 28:309–323
Deodikar GB (1959a) Geographical distribution based on morphological characters (structure of
genitalia and crossability among different bee species). Indian Bee J 23:60–61
16 S.E. Radloff et al.
-
Deodikar GB (1959b) Some taxonomic problems in honeybees. 1. The concept of supra-generic
grouping. Bee World 40:121–124
Deodikar GB (1960) Some indications on the phylogenetic interrelations among bees. Bee Genet
Inf Bull 1:15–16
Deodikar GB, Ghatge AL, Phadke RP, Mahindre DB, Kshirsagar K, Muvel KS, Thakar CV (1977)
Nesting behaviour of Indian honeybees. III. Nesting behaviour of Apis dorsata Fab. IndianBee J 39:1–12
Diniz-Filho JAF, Malapsina O, Pignata MIB (1993) Geographic variation in Apis cerana indica F.:a spatial autocorrelation analysis of morphometric patterns. J Apic Res 32:65–72
Dobzhansky TG (1937) Genetics and the origin of species. Columbia University Press, New York
Dover C (1929) Wasps and bees in the Raffles Museum, Singapore. Bull Raffles’ Museum,
Singapore 2:43–70
Drory E (1888) From my notebook: notes on bees from a trip around the world. Bienenvater
20:20–30 [in German]
Dung PX, Thai PH, Trung LQ (1996) Some comparative characteristics between Apis floreaand Apis andreniformis in Minh Hai Province. In: Proceedings of the 3rd Asian apicultureassociation, Hanoi, p 62
DuPraw EJ (1964) Non-Linnean taxonomy. Nature 202:849–852
Enderlein G (1906) New honeybees and contribution to the distribution of the genus Apis. StettEntomol Ztg 67:331–334 [in German]
Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis).J Hymenopt Res 8:165–196
Engel MS (2006) A giant honey bee from the Middle Miocene of Japan (Hymenoptera: Apidae).
Am Mus Novit 3504:1–12
Engel MS, Schultz TR (1997) Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Ann
Entomol Soc Am 90:43–53
Engel MS, Hinojosa-Diaz IA, Rasnitsyn AP (2009) A honey bee from the Miocene of Nevada
and the biogeography of Apis (Hymenoptera: Apidae; Apini). Proc Calif Acad Sci 60:23–38
Fabricius JC (1787) Mantissa insectorum. Hafniae, Proft [in Latin, cited from Maa 1953]
Fabricius JC (1793) Entomologia systematica emendata et aucta. Secundum classes, ordines,
genera, species adjectis synonimis, locis, observationibus, descriptionibus. Hafniae, Proft
[in Latin, cited from Maa 1953]
Fuchs S, Koeniger N, Tingek S (1996) The morphometric position of Apis nuluensis Tingek,Koeniger and Koeniger, 1996 within cavity-nesting honeybees. Apidologie 27:397–405
Gan YY, Otis GW, Mardan MB, Tan SG (1991) Allozyme diversity in Asian Apis. In: Smith DR(ed) Diversity in the genus Apis. Westview, Boulder, pp 117–130
Garnery L, Vautrin D, Cornuet JM, Solignac M (1991) Phylogenetic relationships in the genus
Apis inferred from mitochondrial DNA sequence data. Apidologie 22:87–92Gerst€acker CEA (1863) On the geographical distribution and varieties of the honeybee, with
remarks upon the exotic honeybees of the old world. Ann Mag Nat Hist 11(270–283):
333–347
Goetze GKL (1964) The honeybee under natural and beekeeping conditions. Part 1. Systematics,
reproduction and heritability. Monogr Angew Entomol 19:1–20 [in German]
Hadisoesilo S, Otis GW (1996) Drone flight times confirm the species status of Apis nigrocinctaSmith, 1861 to be a species distinct from Apis cerana F., 1793, in Sulawesi, Indonesia.Apidologie 27:361–369
Hadisoesilo S, Otis GW (1998) Differences in drone cappings of Apis cerana and Apis nigrocincta.J Apic Res 37:11–15
Hadisoesilo S, Otis GW, Meixner M (1995) Two distinct populations of cavity-nesting honeybees
(Hymenoptera: Apidae) in South Sulawesi, Indonesia. J Kans Entomol Soc 68:399–407
Hadisoesilo S, Meixner M, Ruttner F (1999) Geographic variation within Apis koschevnikoviButtel-Reepen, 1906, in Borneo. Treubia 31:299–306
1 The Asian Species of Apis 17
-
Hadisoesilo S, Raffiudin R, Susanti W, Atmowidi T, Hepburn C, Radloff SE, Fuchs S, Hepburn
HR (2008) Morphometric analysis and biogeography of Apis koschevnikovi Enderlein (1906).Apidologie 39:495–503
Hepburn HR, Smith DR, Radloff SE, Otis GW (2001) Infraspecific categories of Apis cerana:
morphometric, allozymal and mtDNA diversity. Apidologie 32:3–23.
Hepburn HR, Hepburn C (2005) Bibliography of Apis florea. Apidologie 36:377–378Hepburn HR, Hepburn C (2008) Bibliography of Apis koschevnikovi. Apidologie 39:507Hepburn HR, Hepburn C (2009) Bibliography of Apis andreniformis. Apidologie 40:3Hepburn HR, Smith DR, Radloff SE, Otis GW (2001a) Infraspecific categories of Apis cerana:
morphometric, allozymal and mtDNA diversity. Apidologie 32:3–23
Hepburn HR, Radloff SE, Verma S, Verma LR (2001b) Morphometric analysis of Apis ceranapopulations in the southern Himalayan region. Apidologie 32:435–447
Hepburn HR, Radloff SE, Otis GW, Fuchs S, Verma LR, Ken T, Chaiyawong T, Tahmasebi G,
Ebadi R, Wongsiri S (2005) Apis florea: morphometrics, classification and biogeography.Apidologie 36:359–376
Huxley J (1940) The new systematics. Clarendon, Oxford
Jain PC (1967) Morphometrics of bees Apis dorsata F., Apis indica F., Apis florea F., Megachilelanata F., Trigona smithii B. (Hymenoptera: Apidae) and their foraging habits at Udaipur.Thesis, University of Udaipur
Jayavasti S, Wongsiri S (1992) Scanning electron microscopy analysis of honeybees (Apis florea,Apis dorsata, Apis cerana, Apis mellifera, Apis andreniformis and Apis koschevnikovi) stings.Recent Adv Toxicol Res 2:193–204
Keeling CI, Otis GW, Hadisoesilo S, Slessor KN (2001) Mandibular gland component analysis in
the head extracts of Apis cerana and Apis nigrocincta. Apidologie 32:243–252Kirchner WH, Dreller C, Grasser A, Baidya D (1996) The silent dances of the Himalayan
honeybee, Apis laboriosa. Apidologie 27:331–339Koeniger G (1991) Diversity in Apis mating systems. In: Smith DR (ed) Diversity in the genus
Apis. Westview, Boulder, pp 199–212Koeniger N, Koeniger G (1991) An evolutionary approach to mating behaviour and drone
copulatory organs in Apis. Apidologie 22:581–590Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apido-
logie 31:313–339
Koeniger N, Koeniger G (2001) Behavioural mating barriers among sympatric species of the genus
Apis. In: Proceedings of the 7th international conference on apiculture tropical bees, ChiangMai, pp 79–85
Koeniger N, Koeniger G, Gries M, Tingek S, Kelitu A (1996a) Observations on colony defense of
Apis nuluensis Tingek, Koeniger and Koeniger, 1996 and predatory behaviour of the hornet,Vespa multimaculata Pérez, 1910. Apidologie 27:341–352
Koeniger N, Koeniger G, GriesM, Tingek S,Kelitu A (1996b) Reproductive isolation ofApis nuluensisTingek, Koeniger and Koeniger, 1996 by species-specific mating time. Apidologie 27:353–360
Koeniger N, Koeniger G, Tingek S, Kelitu A (1996c) Interspecific rearing and acceptance of
queens between Apis cerana Fabricius, 1793 and Apis koschevnikovi Buttel-Reepen, 1906.Apidologie 27:371–380
Koschevnikov GA (1900–1905) Materials on the natural history of the honeybee. Soc Amateurs
Sci Nat 1–2 [cited from Alapatov 1929]
Kshirsagar KK (1969) Preliminary observations on the biometry of Apis dorsata Fab. queen.Indian Bee J 31:12–16
Kuang BY (1983) Studies on the small black honeybee. Chin Apic 6:10 [in Chinese]
Kuang BY (1986) The species of Apis in China. Apic China 5:7–9 [in Chinese]Kuang BY (2002) Evolution and classification of Apini. J Bee 2:1–2 [in Chinese]
Kuang BY, Li YC (1985) The genus Apis in China. Chinese Beekeep 76:7–9 [in Chinese]Kuang BY, Li YO (1988) Studies on Apini. Sci Agric Sinica 21:85–90 [in Chinese]
18 S.E. Radloff et al.
-
Lavrekhin FA (1935) Contribution to the study of variation of the honeybee. 2. Comparative
biometric characteristics of the sexual appendages of the drones belonging to different forms of
the genus Apis. Zool Zh 14:655–663 [in Russian]Li S, Meng YP, Chang JT, Li JH, He SY, Kuang BY (1986) A comparative study of esterase
isozymes in 6 species of Apis and 9 genera of Apoidea. J Apic Res 25:129–133Li YQ (1984) Discussions on the taxonomy of six species of Apis. J Bee 4:19–21 [in Chinese]Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera,
species, cum characteribus, differentiis, synonymis, locis. Salviae Holmiae Stockholm [in Latin,
cited from Maa 1953]
Lo NH, Gloag RS, Snderson DL, Oldroyd BP (2010) A molecular phylogeny of the genus Apissuggests that the Giant Honey Bee of the Philippines, A. breviligulaMaa, and the Plains HoneyBee of southern India, A. indica Fabricius, are valid species. Syst Entomol 35:226–233
Maa T (1953) An inquiry into the systematics of the tribus Apidini or honeybees (Hym.). Treubia21:525–640
Mathew S, Mathew K (1988) The ‘red’ bees of Sabah. Newsl Beekeep Trop Subtrop Countries
12:10
Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York
McEvoy MV, Underwood BA (1988) The drone and species status of the Himalayan honeybee,
Apis laboriosa (Hymenoptera: Apidae). J Kans Entomol Soc 61:246–249Mogga J, Ruttner F (1988) Apis florea in Africa: source of the founder population. Bee World
69:100–103
Morse RA, Laigo FM (1968) Honeybees in the Philippines. Philipp Biota 3:3–4
Mujumdar S, Kshirsagar KK (1986) Morphometric characterization of Apis dorsata Fabr. workers.Indian Bee J 48:25–29
Muzaffar N, Ahmad R (1989) Distribution and competition of Apis spp. in Pakistan. In: Proceed-ings of the 4th international conference on apiculture in tropical climates, Cairo, pp 449–452
Nanork P, Deowanish S, Wongsiri S (2001) Mitochondrial DNA variability of dwarf honeybee
(Apis florea Fabricius (1787)) in Thailand by using PCR-RFLP technique. In: Proceedings ofthe 7th international conference on tropical bees, Chiang Mai, pp 341–345
Narayanan ES, Sharma PL, Phadke KG (1960) Studies on biometry of the Indian bees II. Tongue
length, wing hooks, worker-brood-cell size and thickness of comb of Apis florea F. at Pusa(Bihar). Indian Bee J 22:81–88
Nunamaker RA, Wilson WT, Ahmad R (1984) Malate dehydrogenase and non-specific esterase
isoenzymes of Apis florea, A. dorsata, and A. cerana detected by isoelectric focusing. J KansEntomol Soc 57:591–595
Oldroyd BP, Rinderer TE, Wongsiri S (1992) Pollen resource partitioning by Apis dorsata, Apiscerana, Apis andreniformis and Apis florea in Thailand. J Apic Res 31:3–7
Ono M (1992) The Asian honeybees (Apis spp.). Honeybee Sci 13:19–22Otis GW (1991) A review of the diversity of species within Apis. In: Smith DR (ed) Diversity in
the genus Apis. Westview, Boulder, pp 29–49Otis GW (1996) Distributions of recently recognized species of honeybees (Hymenoptera: Apidae;
Apis) in Asia. J Kans Entomol Soc 69:311–333Otis GW, Hadisoesilo S (1990) Honeybee survey of South Sulawesi. J Penelitian Kehutanan 4:1–3
Otis GW, Hadisoesilo S, Sugiyani, Cooper AM (2001) Using social bees as indicators of habitat
quality in Sulawesi, Indonesia. In: Proceedings of the 7th international conference on tropical
bees, Chiang Mai, pp 313–317
Özkani A, Gharlek MM, Özden B, Kandemir I (2009) Multivariate morphometric study on Apisflorea distributed in Iran. Turk J Zool 33:93–102
Patinawin S, Wongsiri S (1993) Male genitalia of honey bees. In: Connor LJ, Rinderer TE,
Sylvester HA, Wongsiri S (eds) Asian apiculture. Wicwas, Cheshire, Connecticut, pp 110–116
Peng YS, Nasr ME, Locke SJ (1989) Geographical races of Apis cerana Fabricius in China andtheir distribution. Review of recent Chinese publications and a preliminary statistical analysis.
Apidologie 20:9–20
1 The Asian Species of Apis 19
-
Pesenko YA, Lelei AS, Radchenko VG, Filatkin GN (1989) Chinese wax-bee, Apis ceranacerana F. (Hymenoptera: Apidae) in the Far East of the USSR. Entomol Obozr 68:527–548[in Russian]
Petrov P (1992) Distribution and phylogeny of the honeybee genus Apis (Hymenoptera: Apidae).Uspekhi Sovremennoi Biologii 112:359–372 [in Russian]
Poulton EB (1908) Essays on evolution. Clarendon, Oxford
Radloff SE, Hepburn HR (1998) The matter of sampling distance and confidence levels in the
subspecific classification of honeybees, Apis mellifera L. Apidologie 29:491–501Radloff SE, Hepburn HR (2000) Population structure and morphometric variance in the Apis
mellifera scutellata group of honeybees in Africa. Genet Mol Biol 23:305–316Radloff SE, Hepburn HR (2002) Multivariate morphometric analysis of the Apis cerana popula-
tions of southern Asia. In: Proceedings of the 14th international congress, IUSSI, Sapporo, p 209
Radloff SE, Hepburn HR, Otis GW (2001) Flight machinery of honey bees (Hymenoptera:
Apidae; Apis). In: Proceedings of the 7th international conference on tropical bees, ChiangMai, pp 163–168
Radloff SE, Hepburn HR, Koeniger G (2003a) Comparison of flight design of Asian honeybee
drones. Apidologie 34:353–358
Radloff SE, Hepburn HR, Bangay L (2003b) Quantitative analysis of intercolonial and intracolo-
nial morphometric variance in honeybees, Apis mellifera and Apis cerana. Apidologie34:339–352
Radloff SE, Hepburn HR, Fuchs S (2005a) The morphometric affinities of Apis cerana of theHindu Kush and Himalayan regions of western Asia. Apidologie 36:25–30
Radloff SE, Hepburn HR, Hepburn C, Fuchs S, Otis GW, Sein MM, Aung HL, Pham HT, Tam
DQ, Nuru A, Tan K (2005b) Multivariate morphometric analysis of the Apis cerana popula-tions of mainland southern Asia. Apidologie 36:127–139
Radloff SE, Hepburn HR, Fuchs S, Otis GW, Hadisoesilo S, Hepburn C, Ken T (2005c) Multivar-
iate morphometric analysis of the Apis cerana populations of oceanic Asia. Apidologie36:475–492
Radloff SE, Hepburn C, Hepburn HR, Fuchs S, Hadisoesilo S, Tan K, Engel MS, Kuznetsov V
(2010) Population structure and classification of Apis cerana. Apidologie 41:589–601Raffiudin R, Crozier RH (2007) Phylogenetic analysis of honeybee behavioral evolution. Mol
Phylogenet Evol 43:543–552
Ratnam R (1939) A preliminary study in the biometric variations in the Indian honeybees. Madras
Agric J 27:432–439
Rattanawannee A, Channchao C, Wongsiri S (2008) Morphometric and genetic variation of small
dwarf honeybees Apis andreniformis Smith, 1858 in Thailand. Insect Sci 14:451–460Rensch B (1929) The concept of geographical races and the problem of speciation. Gebr€uder
Borntraeger, Berlin [in German]
Rinderer TE (1988) The rediscovery of Apis koschevnikovi. Am Bee J 128:807Rinderer TE, Koeniger N, Tingek S, Mardan M, Koeniger G (1989) A morphological comparison
of the cavity dwelling honeybees of Borneo Apis koschevnikovi (Buttel-Reepen, 1906) andApis cerana (Fabricius, 1793). Apidologie 20:405–411
Rinderer TE, Oldroyd BP, Wongsiri S, Sylvester HA, de Guzman LI, Potichot S, Sheppard WS,
Buchmann SL (1993) Time of drone flight in four honeybee species in south-eastern Thailand.
J Apic Res 32:27–33
Rinderer TE, Oldroyd BP, Wongsiri S, Sylvester HA, de Guzman LI, Stelzer JA, Riggio RM
(1995) A morphological comparison of the dwarf honeybees of southeastern Thailand and
Palawan, Philippines. Apidologie 26:387–394
Rinderer TE, Wongsiri S, Kuang BY, Liu JS, Oldroyd BP, Sylvester HA, de Guzman LI (1996)
Comparative nest architecture of the dwarf honeybees. J Apic Res 35:19–26
Rinderer TE, Oldroyd BP, de Guzman LI, Wattanachaiyingcharoen W, Wongsiri S (2002) Spatial
distribution of the dwarf honeybees in an agroecosystem in southeastern Thailand. Apidologie
33:539–543
20 S.E. Radloff et al.
-
Roubik DW, Sakagami SF, Kudo I (1985) A note on distribution and nesting of the Himalayan
honeybee Apis laboriosa Smith (Hymenoptera: Apidae). J Kans Entomol Soc 58:746–749Ruttner F (1975) A metatarsal clasping structure in the Apis drone. Entomol Germ 2:22–29Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin
Ruttner F (1992) Naturgeschichte der Honigbienen. Ehrenwirth, Munchen
Ruttner F, Kauhausen D, Koeniger N (1989) Position of the red honey bee, Apis koschevnikovi(Buttel-Reepen 1906), within the genus Apis. Apidologie 20:395–404
Sakagami SF, Matsumura T, Ito K (1980) Apis laboriosa in the Himalaya, the little known worldlargest honeybee (Hymenoptera: Apidae). Insecta Matsumurana 19:47–77
Sakai S, Hoshiba H, Hoshiba E (1986) Integrated taxonomic information on honeybees.
In: Proceedings of the 30th International Congress Apicultural, Nagoya, pp 134–139
Sharma PC (1983) Morphometric studies on Apis florea F. and Apis dorsata F. of HimachalPradesh and Punjab. Thesis, Himachal Pradesh University
Sheppard WS, Berlocher SH (1989) Allozyme variation and differentiation among four Apisspecies. Apidologie 20:419–431
Singh MP, Verma LR, Daly HV (1990) Morphometric analysis of the Indian honeybee in the
northeast Himalayan region. J Apic Res 29:3–14
Smith DR (1991) Mitochondrial DNA and honeybee biogeography. In: Smith DR (ed) Diversity in
the genus Apis. Westview, Boulder, pp 131–176Smith DR (2002) Biogeography of Apis cerana: Southeast Asia and the Indo-Pakistan subconti-
nent. In: Proceedings of the 16th international congress, IUSSI, Sapporo, p 209
Smith DR, Villafuerte L, Otis G, Palmer MR (2000) Biogeography of Apis cerana F. andA. nigrocincta Smith: Insights from mtDNA studies. Apidologie 31:265–280
Smith DR, Palmer MR, Otis GW, Damus M (2003) Mitochondrial DNA and AFLP markers
support species status of Apis nigrocincta. Insectes Soc 50:185–190Smith F (1858) Catalogue of the hymenopterous insects collected at Sarawak, Borneo; Mount
Ophir, Malacca; and at Singapore, by A.R. Wallace. Proc Linn Soc Lond 2:42–130
Smith F (1861) Descriptions of new species of hymenopterous insects collected by A.R. Wallace
at Celebes. Proc Linn Soc Lond 5:57–93
Smith F (1865) On the species and varieties of the honey-bees belonging to the genus Apis. AnnMag Nat Hist 15:372–380
Smith F (1871) A catalogue of the aculeate Hvmenoptcra and Ichneumonidae of India and the
eastern Archipelago. J Linn Soc 11:285–415
Sulistianto A (1990) Morphometric analysis of Indonesian honeybees. Thesis, University of Wales
College, Cardiff
Sylvester HA, Limbipichai K, Wongsiri S, Rinderer TE, MardanMB (1998) Morphometric studies
of Apis cerana in Thailand and the Malaysian peninsula. J Apic Res 37:137–145Szabo TI (1990) Morphometric characteristics of Apis cerana from Sri Lanka. Apidologie
21:505–509
Tahmasebi G, Ebadi R, Tajabadi N, Akhoundi M, Faraji S (2002) The effects of geographical and
climatic conditions on the morphological variation and separation of Iranian small honeybee
(Apis florea F.) populations. J Sci Tech Agric Nat Res 6:169–176Takahashi JI, Nakamura J, Sasaki M, Tingek S, Akimoto SI (2002) New haplotypes for the non-
coding region of mitochondrial DNA in cavity-nesting honey bees Apis koschevnikovi and Apisnuluensis. Apidologie 33:25–31
Tan K, Fuchs S, Ruiguang Z (2002) Morphometrical characterization of Apis cerana inYunnan Province of China. In: Proceedings of the 14th international congress, IUSSI, Sapporo,
p 208
Tan K, Fuchs S, Koeniger N, Ruiguang Z (2003) Morphological characterization of Apis cerana inthe Yunnan province of China. Apidologie 34:553–561
Tanaka H, Roubik DW, Kato M, Liew F, Gunsalam G (2001) Phylogenetic position of Apisnuluensis of northern Borneo and phylogeography of A. cerana as inferred from mitochondrialDNA sequences. Insectes Soc 48:44–51
1 The Asian Species of Apis 21
-
Thakar CV, Tonapi KV (1962) Nesting behaviour of Indian honeybees. II. Nesting habits and
comb cell differentiation in Apis florea Fab. Indian Bee J 24:27–31Thapa R, Shrestha R, Manandhar DN, Bista S, Kafle B (2001) Beekeeping in Nepal. In: Proceed-
ings of the 7th international conference on tropical bees, Chiang Mai, pp 409–413
Tilde AC, Fuchs S, Koeniger N, Cervancia CR (2000) Morphometric diversity of Apis ceranaFabr. within the Philippines. Apidologie 31:249–264
Tingek S, Mardan M, Rinderer TE, Koeniger N, Koeniger G (1988) Rediscovery of Apis vechti(Maa, 1953): the Saban honey bee. Apidologie 19:97–102
Tingek S, Koeniger G, Koeniger N (1996) Description of a new cavity-nesting species of Apis(Apis nuluensis n. sp.) from Sabah, Borneo, with notes on its occurrence and reproductivebiology. Senckenbergiana Biol 76:115–119
Trehan KN, Singh H (1961) Measurements of the tongue and of the worker and drone cells of Apisdorsata Fab. in the Punjab. Indian Bee J 23:31–36
Trung LQ, Dung PX, Ngan TX (1996) A scientific note on first report of Apis laboriosa F Smith,1871 in Vietnam. Apidologie 27:487–488
Underwood BA (1990) The behavior and energetics of high-altitude survival by the Himalayan
honeybee, Apis laboriosa. Thesis, Cornell University, IthacaVerma LR (1992) Species and genetic diversity in Himalayan honeybees. In: Verma LR (ed)
Honeybees in mountain agriculture. Oxford and IBH, New Delhi, pp 39–49
Verma LR, Mattu VK, Daly HV (1994) Multivariate morphometrics of the Indian honeybee in the
northwest Himalayan region. Apidologie 25:203–223
von Buttel-Reepen H (1906) Contributions to the systematics, biology as well as the historical and
geographical distribution of honeybees (Apis mellifica L.) their variability and other Apisspecies. Mitt Zool Mus Berlin 3:117–201 [in German]
Wheeler QD, Meier R (eds) (2000) Species concepts and phylogenetic theory. Columbia Univer-
sity Press, New York
Willis LG, Winston ML, Honda BM (1992) Phylogenetic relationships in the honeybee (genus
Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrialDNA. Mol Phylogenet Evol 1:169–178
Wilson EO, Brown WL (1951) The subspecies concept and its taxonomic implication. Syst Zool
2:97–111
Wongsiri S, Limbipichai K, Tangkanasing P, Mardan M, Rinderer TE, Sylvester HA, Koeniger G,
Otis GW (1990) Evidence of reproductive isolation confirms that Apis andreniformis (Smith,1858) is a separate species from sympatric Apis florea (Fabricius, 1787). Apidologie 21:47–52
Woyke J, Wilde J, Wilde M, Sivaram V, Cervancia C, Nagaraja N, Reddy M (2008) Comparison
of defense body movements of Apis laboriosa, Apis dorsata dorsata and Apis dorsata brevi-ligula honey bees. J Insect Behav 21:481–494
Wu YR, Kuang B (1986) A study of the genusMicrapis (Apidae). Zool Res 7:99–102 [in Chinese]Wu YR, Kuang B (1987) Two species of small honeybee: a study of the genus Micrapis. Bee
World 68:153–155
Yang GH (1986) The distribution of the eastern honeybee (Apis cerana Fab.) in China and ananalysis of its subspecies. J Yunnan Agric Univ 12:202–206 [in Chinese]
Yang GH (2001) The biology of Apis cerana. GH Yang, Beijing [in Chinese]
22 S.E. Radloff et al.
-
Chapter 2
Phylogeny of the Genus Apis
Nikolaus Koeniger, Gudrun Koeniger, and Deborah Smith
2.1 The Early Historical Background
In the middle of eighteenth century, under the influence of Linnaeus’s then new
approach to classification (1758), a stream of exotic specimens of an unexpected
diversity began to reach western museums and collections (Fabricius 1787). This
flow of new material continued in the nineteenth century, the time of the great
explorers and collectors like Alfred Russell Wallace (Smith 1858, 1865). Among
these mainly tropical animals, honeybees received special attention, and based on
colouration, size and other morphological characters, the specimens were classified
and named, resulting in more than 100 different names, many of which referred to
single worker bees deposited in the major collections of natural history museums.
Coincidently during that period, drastic changes in beekeeping took place. The
introduction of the movable frame hive around 1850 started a new epoch in the
relationship between beekeepers and their bees. A new guild of scientific bee-
keepers and beekeeping scientists began to spearhead research. Personalities like
Johann Dzierzon (1849), Baron August von Berlepsch (1873) and others, in close
cooperation with professional biologists like Prof. B.T.E. von Siebold (1856),
described the biological ground plan of A. mellifera and extended knowledge ofcolony structure and honeybee biology. The “acclimatisation” movement, whose
goal it was to augment and “improve” the fauna and flora of a region by introducing
N. Koeniger
Institut f€ur Bienenkunde, (Polytechnische Gesellschaft) Fachbereich Biowissenschaften GoetheUniversit€at, Frankfurt a.M. Karl-von-Frisch-Weg 2, D61440 Oberursel, Germanye-mail: [email protected]
G. Koeniger
Institut f€ur Bienenkunde, Karl-von-Frisch-Weg 2, 61440 Oberursel, Germanye-mail: [email protected]
D. Smith
Department of Ecology and Evolutionary Biology/Entomology, University of Kansas, Haworth
Hall, 1200 Sunnyside Ave, Lawrence, KS 66045, USA
e-mail: [email protected]
H.R. Hepburn and S.E. Radloff (eds.), Honeybees of Asia,DOI 10.1007/978-3-642-16422-4_2, # Springer-Verlag Berlin Heidelberg 2011
23
-
and gradually acclimatising non-native species, also contributed to our understand-
ing of honeybee biology.
Honeybee colonies from several southern regions, not only Mediterranean
countries like Italy, Greece and Cyprus but also Egypt and other African regions,
were imported to Europe (and honeybees from Europe were exported to Africa).
The results of these importations were similar in all cases, where indigenous
A. mellifera populations were naturally present. The imported exotic honeybeesinterbred with the local populations producing fully fertile hybrids. These practical
experiences demonstrated beyond any doubt that African and European honeybee
populations belonged to one species, A. mellifera, and that the impressive varia-bility in colouration, morphology and behaviour among African, Middle East and
European honeybees were differences within one species.
2.2 von Buttel-Reepen to Maa: 1900–1953
2.2.1 H. von Buttel-Reepen (1906)
The conflict between the numerous species names found in the collections of
several natural history museums and the perfect hybridisation of African and
European honeybees was solved by von Buttel-Reepen (1906) in his ground-
breaking treatise on the taxonomy and phylogeny of honeybees. Based on his
solid practical beekeepi